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Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes.

Ragg H, Kumar A, Köster K, Bentele C, Wang Y, Frese MA, Prib N, Krüger O - BMC Evol. Biol. (2009)

Bottom Line: DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously.The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biotechnology, Faculty of Technology and Center for Biotechnology, University of Bielefeld, D-33501 Bielefeld, Germany. hr@zellkult.techfak.uni-bielefeld.de

ABSTRACT

Background: Intron gains reportedly are very rare during evolution of vertebrates, and the mechanisms underlying their creation are largely unknown. Previous investigations have shown that, during metazoan radiation, the exon-intron patterns of serpin superfamily genes were subject to massive changes, in contrast to many other genes.

Results: Here we investigated intron dynamics in the serpin superfamily in lineages pre- and postdating the split of vertebrates. Multiple intron gains were detected in a group of ray-finned fishes, once the canonical groups of vertebrate serpins had been established. In two genes, co-occurrence of non-standard introns was observed, implying that intron gains in vertebrates may even happen concomitantly or in a rapidly consecutive manner. DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.

Conclusion: Multiple intron acquisitions were identified in serpin genes of a lineage of ray-finned fishes, but not in any other vertebrates, suggesting that insertion rates for introns may be episodically increased. The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously. The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site. The association of intron gains in the serpin superfamily with a group of fishes that underwent genome compaction may indicate that DNA breakage/repair processes might foster intron birth.

Show MeSH
Intron-coded classification of serpin genes from vertebrates and lancelets and overview on intron gain positions. Vertebrate serpins are classified into six groups (V1–V6), based on group-specific sets of standard introns (black arrowheads). Characteristic representatives of each group are shown on the right. Non-canonical introns (marked in colors also used to indicate the genes concerned) are exclusively present in a lineage of ray-finned fishes, including Oryzias latipes (Japanese medaka), Gasterosteus aculeatus (stickleback), Tetraodon nigroviridis (green-spotted pufferfish) and Takifugu rubripes (Japanese pufferfish), but not in Petromyzon marinus and Lampetra fluviatilis (lampreys), Danio rerio (zebrafish), and tetrapods. Positions of introns (indicated on top) refer to human α1-antitrypsin, their phases (a-c) are given with respect to their location after the first, second or third base of the codon concerned. For comparison, serpins from lancelets (groups L1 to L3, intron positions indicated by grey arrowheads) have been included, demonstrating that there is little congruence concerning intron positions within the serpin superfamily. The intron at position 262c in group V5 (white arrowhead) is only found in fishes and was possibly lost in tetrapods. Some genes of group V1 lack the 85c intron. Some introns of L3 genes from B. floridae are restricted to individual members of this group (intron 280b: Spn9; introns 224b and 278b: Spn10). Due to alignment problems, the exact positions of the following introns are ambiguous: group V3, intron 86a-90a; group L1, intron 176a; group L2, intron 86b; group L3, intron 175c. Only introns mapping to the conserved serpin scaffold (amino acids 33 to 394 of human α1-antitrypsin) are considered.
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Figure 1: Intron-coded classification of serpin genes from vertebrates and lancelets and overview on intron gain positions. Vertebrate serpins are classified into six groups (V1–V6), based on group-specific sets of standard introns (black arrowheads). Characteristic representatives of each group are shown on the right. Non-canonical introns (marked in colors also used to indicate the genes concerned) are exclusively present in a lineage of ray-finned fishes, including Oryzias latipes (Japanese medaka), Gasterosteus aculeatus (stickleback), Tetraodon nigroviridis (green-spotted pufferfish) and Takifugu rubripes (Japanese pufferfish), but not in Petromyzon marinus and Lampetra fluviatilis (lampreys), Danio rerio (zebrafish), and tetrapods. Positions of introns (indicated on top) refer to human α1-antitrypsin, their phases (a-c) are given with respect to their location after the first, second or third base of the codon concerned. For comparison, serpins from lancelets (groups L1 to L3, intron positions indicated by grey arrowheads) have been included, demonstrating that there is little congruence concerning intron positions within the serpin superfamily. The intron at position 262c in group V5 (white arrowhead) is only found in fishes and was possibly lost in tetrapods. Some genes of group V1 lack the 85c intron. Some introns of L3 genes from B. floridae are restricted to individual members of this group (intron 280b: Spn9; introns 224b and 278b: Spn10). Due to alignment problems, the exact positions of the following introns are ambiguous: group V3, intron 86a-90a; group L1, intron 176a; group L2, intron 86b; group L3, intron 175c. Only introns mapping to the conserved serpin scaffold (amino acids 33 to 394 of human α1-antitrypsin) are considered.

Mentions: In vertebrates, serpin genes are often arranged in tandem arrays and they constitute a substantial fraction of mammalian genomes. During diversification of vertebrates the superfamily has undergone considerable expansion [16,17]. Serpins are unusual compared to most other superfamilies with regards to the dynamics of gene organization. Genes from basal metazoans, such as annelids [18] or sea anemones [19], often share an intron-rich structure with their vertebrate homologues, implying that introns may be stably maintained for hundreds of millions of years. Serpin genes of basal metazoans, in contrast, are not generally intron-rich, and their exon-intron structures are not conserved along the lineages leading to vertebrates. Sporadic investigations of various species revealed radically different intron patterns in serpin genes, indicating that, during diversification of eumetazoans, massive changes in gene architectures have occurred [20,21]. The structures of serpin genes from various vertebrates (Figure 1), however, proved to be strongly conserved, enabling reliable, intron-coded classification of the superfamily into six groups (V1–V6). Generally, there is very little congruence between these groups concerning numbers and positions of introns. Altogether, 25 different intron positions mapping to the serpin scaffold were detected, but none of them is common to the entire superfamily [22].


Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes.

Ragg H, Kumar A, Köster K, Bentele C, Wang Y, Frese MA, Prib N, Krüger O - BMC Evol. Biol. (2009)

Intron-coded classification of serpin genes from vertebrates and lancelets and overview on intron gain positions. Vertebrate serpins are classified into six groups (V1–V6), based on group-specific sets of standard introns (black arrowheads). Characteristic representatives of each group are shown on the right. Non-canonical introns (marked in colors also used to indicate the genes concerned) are exclusively present in a lineage of ray-finned fishes, including Oryzias latipes (Japanese medaka), Gasterosteus aculeatus (stickleback), Tetraodon nigroviridis (green-spotted pufferfish) and Takifugu rubripes (Japanese pufferfish), but not in Petromyzon marinus and Lampetra fluviatilis (lampreys), Danio rerio (zebrafish), and tetrapods. Positions of introns (indicated on top) refer to human α1-antitrypsin, their phases (a-c) are given with respect to their location after the first, second or third base of the codon concerned. For comparison, serpins from lancelets (groups L1 to L3, intron positions indicated by grey arrowheads) have been included, demonstrating that there is little congruence concerning intron positions within the serpin superfamily. The intron at position 262c in group V5 (white arrowhead) is only found in fishes and was possibly lost in tetrapods. Some genes of group V1 lack the 85c intron. Some introns of L3 genes from B. floridae are restricted to individual members of this group (intron 280b: Spn9; introns 224b and 278b: Spn10). Due to alignment problems, the exact positions of the following introns are ambiguous: group V3, intron 86a-90a; group L1, intron 176a; group L2, intron 86b; group L3, intron 175c. Only introns mapping to the conserved serpin scaffold (amino acids 33 to 394 of human α1-antitrypsin) are considered.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2746811&req=5

Figure 1: Intron-coded classification of serpin genes from vertebrates and lancelets and overview on intron gain positions. Vertebrate serpins are classified into six groups (V1–V6), based on group-specific sets of standard introns (black arrowheads). Characteristic representatives of each group are shown on the right. Non-canonical introns (marked in colors also used to indicate the genes concerned) are exclusively present in a lineage of ray-finned fishes, including Oryzias latipes (Japanese medaka), Gasterosteus aculeatus (stickleback), Tetraodon nigroviridis (green-spotted pufferfish) and Takifugu rubripes (Japanese pufferfish), but not in Petromyzon marinus and Lampetra fluviatilis (lampreys), Danio rerio (zebrafish), and tetrapods. Positions of introns (indicated on top) refer to human α1-antitrypsin, their phases (a-c) are given with respect to their location after the first, second or third base of the codon concerned. For comparison, serpins from lancelets (groups L1 to L3, intron positions indicated by grey arrowheads) have been included, demonstrating that there is little congruence concerning intron positions within the serpin superfamily. The intron at position 262c in group V5 (white arrowhead) is only found in fishes and was possibly lost in tetrapods. Some genes of group V1 lack the 85c intron. Some introns of L3 genes from B. floridae are restricted to individual members of this group (intron 280b: Spn9; introns 224b and 278b: Spn10). Due to alignment problems, the exact positions of the following introns are ambiguous: group V3, intron 86a-90a; group L1, intron 176a; group L2, intron 86b; group L3, intron 175c. Only introns mapping to the conserved serpin scaffold (amino acids 33 to 394 of human α1-antitrypsin) are considered.
Mentions: In vertebrates, serpin genes are often arranged in tandem arrays and they constitute a substantial fraction of mammalian genomes. During diversification of vertebrates the superfamily has undergone considerable expansion [16,17]. Serpins are unusual compared to most other superfamilies with regards to the dynamics of gene organization. Genes from basal metazoans, such as annelids [18] or sea anemones [19], often share an intron-rich structure with their vertebrate homologues, implying that introns may be stably maintained for hundreds of millions of years. Serpin genes of basal metazoans, in contrast, are not generally intron-rich, and their exon-intron structures are not conserved along the lineages leading to vertebrates. Sporadic investigations of various species revealed radically different intron patterns in serpin genes, indicating that, during diversification of eumetazoans, massive changes in gene architectures have occurred [20,21]. The structures of serpin genes from various vertebrates (Figure 1), however, proved to be strongly conserved, enabling reliable, intron-coded classification of the superfamily into six groups (V1–V6). Generally, there is very little congruence between these groups concerning numbers and positions of introns. Altogether, 25 different intron positions mapping to the serpin scaffold were detected, but none of them is common to the entire superfamily [22].

Bottom Line: DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously.The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biotechnology, Faculty of Technology and Center for Biotechnology, University of Bielefeld, D-33501 Bielefeld, Germany. hr@zellkult.techfak.uni-bielefeld.de

ABSTRACT

Background: Intron gains reportedly are very rare during evolution of vertebrates, and the mechanisms underlying their creation are largely unknown. Previous investigations have shown that, during metazoan radiation, the exon-intron patterns of serpin superfamily genes were subject to massive changes, in contrast to many other genes.

Results: Here we investigated intron dynamics in the serpin superfamily in lineages pre- and postdating the split of vertebrates. Multiple intron gains were detected in a group of ray-finned fishes, once the canonical groups of vertebrate serpins had been established. In two genes, co-occurrence of non-standard introns was observed, implying that intron gains in vertebrates may even happen concomitantly or in a rapidly consecutive manner. DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.

Conclusion: Multiple intron acquisitions were identified in serpin genes of a lineage of ray-finned fishes, but not in any other vertebrates, suggesting that insertion rates for introns may be episodically increased. The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously. The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG upward arrowN, previously proposed to serve as intron insertion site. The association of intron gains in the serpin superfamily with a group of fishes that underwent genome compaction may indicate that DNA breakage/repair processes might foster intron birth.

Show MeSH